USP17 is required for clathrin mediated endocytosis of epidermal growth factor receptor

Oncotarget

Volumn 5, Issue 16, 2014, Pages 6964-6975

  Jaworski, Jakub ^a   de la Vega, Michelle ^b   Fletcher, Sarah J ^c   McFarlane, Cheryl ^b   Greene, Michelle K ^a   Smyth, Andrew W ^a   Van Schaeybroeck, Sandra ^b   Johnston, James A ^b,d   Scott, Christopher J ^a   Rappoport, Joshua Z ^c   Burrows, James F ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d AMGEN INC   (United States)

Author keywords

Clathrin; Deubiquitinating; Endocytosis; Epidermal growth factor receptor; USP17

Indexed keywords

CLATHRIN; COLONY STIMULATING FACTOR; DEUBIQUITINASE; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEINASE; RAS CONVERTING ENZYME 1; TRANSFERRIN; TRANSFERRIN RECEPTOR; UBIQUITIN; UNCLASSIFIED DRUG; USP17 PROTEIN; EGFR PROTEIN, HUMAN; USP17L2 PROTEIN, HUMAN;

ARTICLE; CELL MEMBRANE; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME REGULATION; HUMAN; HUMAN CELL; INTERNALIZATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; UBIQUITINATION; GENETIC TRANSFECTION; GENETICS; HELA CELL LINE; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL PROLIFERATION; CLATHRIN; ENDOCYTOSIS; ENDOPEPTIDASES; HELA CELLS; HUMANS; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSFECTION; UBIQUITIN;

EID: 84907065345     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2165     Document Type: Article

References (52)

1. Nijman SM, Luna-Vargas M, Velds A, Brummelkamp TR, Dirac AM, Sixma TK, Bernards R. A genomic and functional inventory of deubiquitinating enzymes. Cell. 2005; 123: 773-786.
2. Fraile JM, Quesada V, Rodri´guez D, Freije JM, Lo´pez-Oti´n C. Deubiquitinases in cancer: new functions and therapeutic options. Oncogene. 2012; 31: 2373-2388.
3. Zhu Y, Os Pless M, Inhorn R, Mathey-Prevot B, D'Andrea AD. The murine DUB-1 gene is specifically induced by the betac subunit of interleukin-3 receptor. Mol Cell Biol. 1996; 16: 4808-4819.
4. Zhu Y, Lambert K, Corless C, Copeland NG, Gilbert DJ, Jenkins NA, D'Andrea AD. DUB-2 is a member of a novel family of cytokine-inducible deubiquitinating enzymes. J Biol Chem. 1997; 272: 51-57.
5. Burrows JF, McGrattan MJ, Rascle A, Humbert M, Baek KH, Johnston JA. DUB-3, a cytokine-inducible deubiquitinating enzyme that blocks proliferation. J Biol Chem. 2004; 279: 13993-14000.
6. de la Vega M, Kelvin AA, Dunican DJ, McFarlane C, Burrows JF, Jaworski J, Stevenson NJ, Dib K, Rappoport JZ, Scott CJ, Johnston JA. The deubiquitinating enzyme USP17 is essential for GTPase subcellular localization and cell motility. Nat Commun. 2011; 2: 259.
7. McFarlane C, Kelvin AA, de la Vega MA, Govender U, Scott CJ, Burrows JF, Johnston JA. The deubiquitinating enzyme USP17 is cell cycle regulated and mediates G1-S transition. Cancer Res. 2010; 70: 3329-3339.
8. Pereg Y, Liu BY, O'Rourke KM, Sagolla M, Dey A, Komuves L, French DM, Dixit VM. Ubiquitin hydrolase Dub3 promotes oncogenic transformation by stabilizing Cdc25A. Nature Cell Biology. 2010; 12: 400-406.
9. van der Lan S, Tsanov N, Crozet C, Maiorano D. High Dub3 Expression in Mouse ESCs Couples the G1/S Checkpoint to Pluripotency. Mol Cell. 2013; 52: 366-379.
10. Burrows JF, Kelvin AA, McFarlane C, Burden RE, McGrattan MJ, de la Vega M, Govender U, Quinn DJ, Dib K, Gadina M, Johnston JA. USP17 regulates Ras activation and cell proliferation by blocking RCE1 activity. J Biol Chem. 2009; 284: 9587-9595.
11. de la Vega MA, Burrows JF, McFarlane C, Govender U, Scott CJ, Johnston JA. The deubiquitinating enzyme USP17 blocks N-Ras membrane trafficking and activation, but leaves K-Ras unaffected. J Biol Chem. 2010; 285: 12028-12036.
12. Jaworski J, Govender U, McFarlane C, de la Vega M, Greene MK, Rawlings ND, Johnston JA, Scott CJ, Burrows JF. A novel RCE1 isoform is required for H-Ras plasma membrane localization and is regulated by USP17. Biochem J. 2014; 457: 289-300.
13. Ramakrishna S, Suresh B, Lee EJ, Lee HJ, Ahn WS, Baek KH. Lys-63-specific deubiquitination of SDS3 by USP17 regulates HDAC activity. J Biol Chem. 2011; 286: 10505-10514.
14. Chen R, Zhang L, Zhong B, Tan B, Liu Y, Shu HB. The ubiquitin-specific protease 17 is involved in virus-triggered type I IFN signaling. Cell Res. 2010; 20: 802-811.
15. Meenhuis A, Verwijmeren C, Roovers O, Touw IP. The deubiquitinating enzyme DUB2A enhances CSF3 signalling by attenuating lysosomal routing of the CSF3 receptor. Biochem J. 2011; 434: 343-351.
16. Rappoport JZ, Simon SM. Endocytic trafficking of activated EGFR is AP-2 dependent and occurs through preformed clathrin spots. J Cell Sci. 2009; 122: 1301-1305.
17. Sorkin A, Goh LK. Endocytosis and intracellular trafficking of ErbBs. Exp Cell Res. 2008; 314: 3093-3106.
18. Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, Nibert ML, Kirchhausen T. Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell. 2004; 118: 591-605.
19. McMahon HT, Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol. 2011; 12: 517-533.
20. Barbieri MA, Heath CM, Peters EM, Wells A, Davis JN, Stahl PD. Phosphatidylinositol-4-phosphate 5-kinase-1beta is essential for epidermal growth factor receptor-mediated endocytosis. J Biol Chem. 2001; 276: 47212-47216.
21. Padro´n D, Wang YJ, Yamamoto M, Yin H, Roth MG. Phosphatidylinositol phosphate 5-kinase Ibeta recruits AP-2 to the plasma membrane and regulates rates of constitutive endocytosis. J Cell Biol. 2003; 162: 693-701.
22. Clague MJ, Urbe S. Endocytosis: the DUB version. Trends in Cell biology. 2006; 16: 551-559.
23. Levkowitz G, Waterman H, Zamir E, Kam Z, Oved S, Langdon WY, Beguinot L, Geiger B, Yarden Y. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 1998; 12: 3663-3674.
24. Urbe S, Sachse M, Row PE, Preisinger C, Barr FA, Strous G, Klumperman J, Clague MJ. The UIM domain of Hrs couples receptor sorting to vesicle formation. J. Cell Sci. 2003; 116: 4169-4179.
25. Williams RL, Urbe S. The emerging shape of the ESCRT machinery. Nat Rev Mol Cell Biol. 2007; 8: 355-368.
26. Row PE, Prior IA, McCullough J, Clague MJ, Urbe S. The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation. J Biol Chem. 2006; 281: 12618-12624.
27. Bowers K, Piper SC, Edeling MA, Gray SR, Owen DJ, Lehner PJ, Luzio JP. Degradation of endocytosed epidermal growth factor and virally ubiquitinated major histocompatibility complex class I is independent of mammalian ESCRTII. J. Biol. Chem. 2006; 281: 5094-5105.
28. Mizuno E, Kobayashi K, Yamamoto A, Kitamura N, Komada M. A deubiquitinating enzyme UBPY regulates the level of protein ubiquitination on endosomes. Traffic. 2006; 7: 1017-1031.
29. Niendorf S, Oksche A, Kisser A, Lo¨hler J, Prinz M, Schorle H, Feller S, Lewitzky M, Horak I, Knobeloch KP. Essential role of ubiquitin-specific protease 8 for receptor tyrosine kinase stability and endocytic trafficking in vivo. Mol. Cell Biol. 2007; 27: 5029-5039.
30. Meijer IMJ, van Leeuwen JEM. ERBB2 is a target for USP8-mediated deubiquitination. Cellular Signalling. 2011; 23: 458-467.
31. Hasdemir B, Murphy JE, Cottrell GS, Bunnett NW. Endosomal deubiquitinating enzymes control ubiquitination and down-regulation of protease-activated receptor 2. J Biol Chem. 2009; 284: 28453-28466.
32. Hislop JN, Henry AG, Marchese A, von Zastrow M. Ubiquitination regulates proteolytic processing of G protein-coupled receptors after their sorting to lysosomes. J. Biol. Chem. 2009; 284: 19361-19370.
33. Berlin I, Higginbotham KM, Dise RS, Sierra MI, Nash PD. The deubiquitinating enzyme USP8 promotes trafficking and degradation of the chemokine receptor 4 at the sorting endosome. J Biol Chem. 2010; 285: 37895-37908.
34. Burrows JF, Johnston JA. Regulation of cellular responses by deubiquitinating enzymes: an update. Front Biosci. 2012; 17: 1184-1200.
35. Galperin E, Sorkin A. Endosomal targeting of MEK2 requires RAF, MEK kinase activity and clathrin-dependent endocytosis. Traffic. 2008; 9: 1776-1780.
36. Wong ES, Fong CW, Lim J, Yusoff P, Low BC, Langdon WY, Guy GR. Sprouty2 attenuates epidermal growth factor receptor ubiquitylation and endocytosis, and consequently enhances Ras/ERK signalling. EMBO J. 2002; 21: 4796-4808.
37. Jones S, Cunningham DL, Rappoport JZ, Heath JK. The non-receptor tyrosine kinase Ack1 regulates the fate of activated EGFR by inducing trafficking to the p62/NBR1 pre-autophagosome J Cell Sci. 2014; 127: 994-1006.
38. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, Di Fiore PP, Polo S. Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci USA. 2005; 102: 2760-2765.
39. Neel NF, Schutyser E, Sai J, Fan G-H, Richmond A. Chemokine receptor internalization and intracellular trafficking. Cytokine & Growth Factor Reviews. 2005; 16: 637-658.
40. Yang W, Wang D, Richmond A. Role of clathrin-mediated endocytosis in CXCR2 sequestration, resensitization, and signal transduction. J Biol Chem. 1999; 274: 11328-11333.
41. Fan G-H, Yang W, Wang X-J, Qian Q, Richmond A. Identification of a motif in the carboxyl terminus of CXCR2 that is involved in adaptin 2 binding and receptor internalization. Biochemistry. 2001; 40: 791-800.
42. Friedrich K, Kammer W, Erhardt I, Bra¨ndlein S, Arnold S, Sebald W. The two subunits of the interleukin-4 receptor mediate independent and distinct patterns of ligand endocytosis. Eur J Biochem. 1999; 265: 457-465.
43. Graeve L, Korolenko TA, Hemmann U, Weiergra¨ber O, Dittrich E, Heinrich PC. A complex of the soluble interleukin-6 receptor and interleukin-6 is internalized via the signal transducer gp130. FEBS Lett. 1996; 399: 131-134.
44. 2 synthesis, which modulates vinculin localisation and neurite dynamics. J Cell Sci. 2010; 123: 3535-3546.
45. Weernink PA, Meletiadis K, Hommeltenberg S, Hinz M, Ishihara H, Schmidt M, Jakobs KH. Activation of type I phosphatidylinositol 4-phosphate 5-kinase isoforms by the Rho GTPases, RhoA, Rac1, and Cdc42. J Biol Chem. 2004; 279: 7840-7849.
46. Fielding AB, Willox AK, Okeke E, Royle SJ. Clathrin-mediated endocytosis is inhibited during mitosis. Proc Natl Acad Sci U S A. 2012; 109: 6572-6577.
47. Schweitzer JK, Burke EE, Goodson HV, D'Souza-Schorey C. Endocytosis resumes during late mitosis and is required for cytokinesis. J Biol Chem. 2005; 280: 41628-41635.
48. Royale SJ. The role of clathrin in mitotic spindle organisation. J Cell Sci. 2012; 125:19-28.
49. Liu L, Shi H, Chen X, Wang Z. Regulation of EGF-stimulated EGF receptor endocytosis during M phase. Traffic. 2011; 12: 201-217.
50. McFarlane C, McFarlane S, Paul I, Arthur K, Scheaff M, Kerr K, Stevenson M, Fennell DA, Johnston JA. The deubiquitinating enzyme USP17 is associated with non-small cell lung cancer (NSCLC) recurrence and metastasis. Oncotarget. 2013; 4: 1836-1843.
51. Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell. 2008; 15: 209-219.
52. Chung BM, Raja SM, Clubb RJ, Tu C, George M, Band V, Band H. Aberrant trafficking of NSCLC-associated EGFR mutants through the endocytic recycling pathway promotes interaction with Src. BMC Cell Biology. 2009; 10: 84. .